POLAR-guided signalling complex assembly and localization drive asymmetric cell division

Houbaert, Anaxi; Zhang, Cheng; Tiwari, Manish; Wang, Kun; Marcos, Alberto de; Savatin, Daniel V.; Urs, Mounashree J.; Zhiponova, Miroslava; Gudesblat, Gustavo E.; Vanhoutte, Isabelle; Eeckhout, Dominique; Boeren, Sjef; Karimi, Mansour; Betti, Camilla; Jacobs, Thomas B.; Fenoll, Carmen; Mena, Montaña; Vries, Sven de; Jaeger, Geert De; Russinova, Eugenia

doi:10.1038/s41586-018-0714-x

Cited by 162 publications

(225 citation statements)

References 38 publications

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“…BASL depends on MAPK phosphorylation for its peripheral polarization before asymmetric division, then, biases the capacity for MAPK signaling towards the SLGC post-division by sequestering the upstream MAPKKK, YODA in the larger daughter (Zhang et al, 2015). POLAR, through its binding of BIN2, changes the nuclear/cytoplasmic balance of the latter, with consequences to MAPK signaling and ultimately to the stability of SPCH in meristemoids post-division (Houbaert et al, 2018). Both MAPK and BIN2-related signaling cascades are used in a large number of developmental and physiological events, and other scaffolds have been identified, perhaps most interesting among them is OCTOPUS (OPS) that, similar to POLAR, sequesters BIN2 away from the nucleus from its a polarized plasma-membrane location in protophloem cells (Vatén et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

“…Does the BRX family work with BASL in regulating MAPKs, or does it scaffold yet another kinase family in the stomatal lineage? There is currently no evidence for direct BIN2-BRXf interactions (Houbaert et al, 2018), nor for MAPK-BRXf interactions (J. Dong, pers.…”

Section: Discussionmentioning

confidence: 99%

“…1A). POLAR affects the nuclear/cytoplasmic ratio of the GSK3b kinase BRASSINOSTEROID INSENSITIVE2 (BIN2), leading to preferential activities at the cell cortex before asymmetric divisions (Houbaert et al, 2018). Both BIN2 and MAPKs target the transcription factor SPEECHLESS (SPCH), leading to its preferential degradation in one daughter of the asymmetric division (Lampard et al, 2008), but BIN2 can also target MAPKs, leading to attenuation of this activity.…”

Section: Introductionmentioning

confidence: 99%

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A Plant-Specific Polarity Module Establishes Cell Fate Asymmetry in the Arabidopsis Stomatal Lineage

Rowe

Dong

Weimer

et al. 2019

Preprint

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Generating cell polarity in anticipation of asymmetric cell division is required in many developmental contexts across a diverse range of species. Physical and genetic diversity among major multicellular taxa, however, demand different molecular solutions to this problem. The Arabidopsis stomatal lineage displays asymmetric, stem cell-like and oriented cell divisions, which require the activity of the polarly localized protein, BASL. Here we identify the plant-specific BREVIS RADIX (BRX) family as localization and activity partners of BASL. We show that members of the BRX family are polarly localized to peripheral domains in stomatal lineage cells and that their collective activity is required for asymmetric cell divisions. We further demonstrate a mechanism for these behaviors by uncovering mutual, yet unequal dependencies of BASL and the BRX family for each other's localization and segregation at the periphery of stomatal lineage cells.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A Plant-Specific Polarity Module Establishes Cell Fate Asymmetry in the Arabidopsis Stomatal Lineage

Rowe

Dong

Weimer

et al. 2019

Preprint

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“…All entry clones were sequence verified. The BIN2 entry plasmid was kindly provided by Jenny Russinova (Houbaert et al, 2018). Entry clones were combined in a Gateway® LR recombination reaction with an empty BiFC destination vector and selected using LB containing spectinomycin and Xgal.…”

Section: Methodsmentioning

confidence: 99%

Establishment of Proximity-dependent Biotinylation Approaches in Different Plant Model Systems

Arora

Abel

Liu

et al. 2019

Preprint

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35Proximity-dependent biotin labelling (PDL) uses a promiscuous biotin ligase (PBL) or a 36 peroxidase fused to a protein of interest. This enables covalent biotin labelling of proteins and 37 allows subsequent capture and identification of interacting and neighbouring proteins without 38 the need for the protein complex to remain intact. To date, only few papers report on the use of 39 PDL in plants. Here we present the results of a systematic study applying a variety of PDL 40 approaches in several plant systems using various conditions and bait proteins. We show that 41TurboID is the most promiscuous variant in several plant model systems and establish protocols 42 which combine Mass Spectrometry-based analysis with harsh extraction and washing 43 conditions. We demonstrate the applicability of TurboID in capturing membrane-associated 44 protein interactomes using Lotus japonicus symbiotically active receptor kinases as test-case. 45We further benchmark the efficiency of various PBLs in comparison with one-step affinity 46 purification approaches. We identified both known as well as novel interactors of the endocytic 47Protein-protein interaction (PPI) studies often fail to capture low-affinity interactions as these 53 are usually not maintained following cell lysis, protein extraction and protein complex 54 purification. Particularly, this is the case for PPI's of integral membrane proteins because of 55 the harsh conditions during protein extraction and purification. Proximity-dependent biotin 56 labelling (PDL) on the contrary, uses covalent biotinylation of proteins that are interactors or 57 near-neighbours of a bait protein of interest in vivo (Varnaite and MacNeill, 2016). Hence, to 58 identify interactions, they do not need to remain intact during purification. Although biotin is 59 an essential cofactor for a small number of omnipresent biotin-dependent enzymes involved 60 mainly in the transfer of CO2 during HCO3 --dependent carboxylation reactions, biotinylation 61 is a relatively rare in vivo protein modification. Moreover, biotinylated proteins can be 62 selectively isolated with high affinity using streptavidin-biotin pairing. PDL, therefore, permits 63

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“…Also Arabidopsis meristemoids exhibit strong asymmetry and polarity, which seems to be important for stomatal spacing and patterning (Lau and Bergmann, 2012;Pillitteri and Torii, 2012), and creates flexibility regarding the relative numbers of stomata and pavement cells, a process modulated by cytokinin (Vat en et al, 2018). Meristemoid polarity in Arabidopsis involves BREAKING OF ASYMME-TRY IN THE STOMATAL LINEAGE (AtBASL; Dong et al, 2009), BREVIS RADIX (AtBRX)-like family genes (Rowe et al, 2019) and AtPOLAR family genes (Houbaert et al, 2018). A striking difference is that the asymmetric division in SMCs is oriented towards the polarity domain in grasses (i.e.…”

Section: Recruiting Subsidiary Cellsa Tale Of Extreme Polarity and Momentioning

confidence: 99%

Form, development and function of grass stomata

2019

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Summary Stomata are cellular breathing pores on leaves that open and close to absorb photosynthetic carbon dioxide and to restrict water loss through transpiration, respectively. Grasses (Poaceae) form morphologically innovative stomata, which consist of two dumbbell‐shaped guard cells flanked by two lateral subsidiary cells (SCs). This ‘graminoid’ morphology is associated with faster stomatal movements leading to more water‐efficient gas exchange in changing environments. Here, we offer a genetic and mechanistic perspective on the unique graminoid form of grass stomata and the developmental innovations during stomatal cell lineage initiation, recruitment of SCs and stomatal morphogenesis. Furthermore, the functional consequences of the four‐celled, graminoid stomatal morphology are summarized. We compile the identified players relevant for stomatal opening and closing in grasses, and discuss possible mechanisms leading to cell‐type‐specific regulation of osmotic potential and turgor. In conclusion, we propose that the investigation of functionally superior grass stomata might reveal routes to improve water‐stress resilience of agriculturally relevant plants in a changing climate.

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POLAR-guided signalling complex assembly and localization drive asymmetric cell division

Cited by 162 publications

References 38 publications

A Plant-Specific Polarity Module Establishes Cell Fate Asymmetry in the Arabidopsis Stomatal Lineage

A Plant-Specific Polarity Module Establishes Cell Fate Asymmetry in the Arabidopsis Stomatal Lineage

Establishment of Proximity-dependent Biotinylation Approaches in Different Plant Model Systems

Form, development and function of grass stomata

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